1. Laurie S. Stevison Suzanne E. McGaugh Mohamed A. F. Noor
Why the association between interspecies divergence and inversions in Drosophila?
Laurie S. Stevison
Suzanne E. McGaugh
Mohamed A. F. Noor

2. Recombination maintains cohesion of species
Species are “groups of alleles in long-term association” – linkage disequilibrium
Similar to some definitions of species
Implicit in other definitions of species
Stopping recombination maintains distinct (haplo)types

3. Chromosome inversions “prevent” recombination between types
Problems with chromosomal pairing
Single crossovers lead to acentric or dicentric chromosomes

4. Chromosome inversions “prevent” recombination between types
Problems with chromosomal pairing
Single crossovers lead to acentric or dicentric chromosomes
Maybe help maintain species?

5. Test system: Drosophila pseudoobscura /D. persimilis
Morphologically identical
Hybrid females fertile (though males sterile)
Overlapping range/ hybridize at low level
Extensive genome sequence data

6. Inversions may have kept Drosophila pseudoobscura and D
Inversions may have kept Drosophila pseudoobscura and D. persimilis apart
>10 years of research summarized here:
Genetic mapping of differences:
Everything maps to 3 inverted regions
Hybrid male sterility
Mate preference
Courtship song
When studying nonhybridizing population, effects map outside inversions, too.

7. Inversions may have kept Drosophila pseudoobscura and D
Inversions may have kept Drosophila pseudoobscura and D. persimilis apart
Inverted regions show higher sequence difference than non-inverted regions
Dpse-Dper looks like Dpse-Dpse when get >2.5Mb from inversion

8. Inversions may have kept Drosophila pseudoobscura and D
Inversions may have kept Drosophila pseudoobscura and D. persimilis apart
Yellow: inverted regions
Blue: collinear regions
Complete suppression of recombination products until ~2.5 megabases outside inversion
Within species, 2.5 megabases would experience >10% recombination

9. Inversions may have kept Drosophila pseudoobscura and D
Inversions may have kept Drosophila pseudoobscura and D. persimilis apart!
Trait differences map to inverted regions in hybridizing populations
Don’t see similar association in non-hybridizing populations
Higher differentiation in inverted than non-inverted regions
Domain of effect of inverted region matches domain of effect on recombination
So… are we done?
One fly in the ointment…

10. Simulation study raises questions…
Inversions don’t completely stop gene flow
Do get double-crossover or gene conversion exchange in inverted region
Over long time, low gene flow often erodes sequence differences within inverted regions
Figure is one of the “best” case-scenarios

11. Conclusions…
“the low levels of recombination within an inversion often result in the loss of accentuated divergence in inverted regions compared to collinear ones” (2009)
“the effects of chromosomal rearrangements can be transient and will be quantitative and not qualitative” (Feder et al 2011)

12. Model Results ≠ Experimental Results
Model says unlikely to see (sustained) difference in inverted region
Data show difference associated with inverted region
and no indication that sympatry is very recent
Both are “right”– what’s up?

13. Some explanations suggested by Feder & Nosil
More exchange in center than near breakpoints
Inversion association stems from breakpoint areas
Clustering of loci within some regions
Very recent secondary contact/ gene flow
Mapping ascertainment bias
Mixed geographic mode of speciation may help

14. Study a matching intra- and inter-species inversion difference!

15. What MIGHT we find? A<B because B linked to inversion
D<C if have “double crossovers” in center of inverted region
In hybrids, ~1/10,000 progeny have double crossovers (L. Stevison)

16. What do we find? Interspecies
A << B ≤ D ≤ C
Regions far outside inversion (A) have low sequence divergence
All regions near or within inversion (B, C, D) have high sequence divergence

17. What do we find? Intraspecies
A ≤ B ≤ D << C
Regions near inversion but inside (C) have high divergence
All regions far, near, or centrally within inversion (A, B, D) low

18. Intraspecies and Interspecies patterns differ…
Divergence
Divergence

19. Intraspecies and Interspecies patterns differ…
Effects of “rare events” cause difference?
BOTH: Rare double-crossovers (10-5)
BOTH: Low crossover rate just outside inversion (10-5?)
INTER: Low rate of hybridization (10-5)

20. Interaction of hybridization and recombination rates matters!
WITHIN SPECIES– Rare exchanges in center and outside breakpoint make little divergence persist
Fits model: recombination rate even higher, 10-5, but that was “maximum” in center of largest inversion
BETWEEN SPECIES– Rare exchanges x rare hybridization allows divergence to persist even in areas of low (but non-zero) recombination
Exchange rate low: 10-5 x 10-5 = 10-10

21. Resolution
Inversions were important in the persistence of Drosophila pseudoobscura & D. persimilis
Possible reason for high divergence persisting in inverted regions is migration rate extremely low: rare2 effect
Importance of descriptive natural history
Relied on pre-1985 field estimates of hybridization rate to get to this important conclusion

22. Punchline: efficacy of inversions in allowing hybridizing species to persist is affected by hybridization rate: - If high, inversion effect decays - If low, inversion effect persists
Thank you!